Gene duplication provides an important source of genetic raw material for phenotypic diversification, but few studies have detailed the mechanisms through which duplications produce evolutionary novelty within species. Here, we investigate how a set of recently duplicated homologs of the floral inducer FLOWERING LOCUS T (FT) has contributed to sunflower domestication. We find that changes in expression of these duplicates are associated with differences in flowering behavior between wild and domesticated sunflower. In addition, we present genetic and functional evidence demonstrating that a frameshift mutation in one paralog, Helianthus annuus FT 1 (HaFT1), underlies a major QTL for flowering time and experienced a selective sweep during early domestication. Notably, this dominant-negative allele delays flowering through interference with action of another paralog, HaFT4. Together, these data reveal that changes affecting the expression, sequence, and gene interactions of HaFT paralogs have played key roles during sunflower domestication. Our findings also illustrate the important role that evolving interactions between new gene family members may play in fostering phenotypic change.